Widespread episodic thiamine deficiency in Northern Hemisphere wildlife

Balk, L.; Hägerroth, P.-Å.; Gustavsson, H.; Sigg, L.; Åkerman, G.; Ruiz Muñoz, Y.; Honeyfield, D.C.; Tjärnlund, U.; Oliveira, K.; Ström, K.; McCormick, S.D.; Karlsson, S.; Ström, M.; van Manen, M.; Berg, A.-L.; Halldórsson, H.; Strömquist, J.; Collier, T.K.; Börjeson, H.; Mörner, T.; Hansson, T.
2016 | Sci Rep | 6 (38821) (1-13)

Many wildlife populations are declining at rates higher than can be explained by known threats to biodiversity. Recently, thiamine (vitamin B1) deficiency has emerged as a possible contributing cause. Here, thiamine status was systematically investigated in three animal classes: bivalves, ray-finned fishes, and birds. Thiamine diphosphate is required as a cofactor in at least five life-sustaining enzymes that are required for basic cellular metabolism. Analysis of different phosphorylated forms of thiamine, as well as of activities and amount of holoenzyme and apoenzyme forms of thiamine-dependent enzymes, revealed episodically occurring thiamine deficiency in all three animal classes. These biochemical effects were also linked to secondary effects on growth, condition, liver size, blood chemistry and composition, histopathology, swimming behaviour and endurance, parasite infestation, and reproduction. It is unlikely that the thiamine deficiency is caused by impaired phosphorylation within the cells. Rather, the results point towards insufficient amounts of thiamine in the food. By investigating a large geographic area, by extending the focus from lethal to sublethal thiamine deficiency, and by linking biochemical alterations to secondary effects, we demonstrate that the problem of thiamine deficiency is considerably more widespread and severe than previously reported.

Thiamine deficiency affecting wildlife health in the Baltic Sea area

Mörner, T.; Hägerroth, P.-Å.; Hansson, T.; Tjärnlund, U.; Gustavsson, H.; Åkerman, G.; Balk, L.
2013 | Wildlife Disease Association (WDA)

The 62nd International Conference of the Wildlife Disease Association | July 27, 2013 | Knoxville, Tennessee, USA

Thiamine (vitamin B1) is synthesized in plants, fungi, and bacteria and is essential for all fish and bird species. Thiamine deficiency causes metabolic disorders in several subcellular compartments, such as the cytosol, mitochondria, and peroxisomes. Clinical symptoms include ataxia, convulsions, paralysis, immune suppression, behavioral and memory disorders, reduced feeding, and anorexia. In the Baltic Sea salmon (Salmo salar), thiamine deficiency has been observed since 1974. This disorder has been named the M74 syndrome. It occurs in episodes affecting the reproduction in 10–90% of the females, depending on year and river. The disorder causes neurological disturbances and histopathological changes in the brain, muscles and kidneys, both in the yolk-sac fry and in the adults.

Recently, thiamine deficiency has also been demonstrated in adults, newly hatched young, and eggs of herring gulls (Larus argentatus), and common eider (Somateria mollissima) in connection with extensive paralysis and mortality in bird colonies in the Baltic Sea area. We have observed in these colonies reproductive disorders, with a reduced number of laid eggs, and high mortality (> 90 percent) in eider ducklings during their first week of life. The many observations of advanced thiamine deficiency in adult birds imply that a varying degree of moderate thiamine deficiency occurs among the affected species. This might be an explanation for the observed increased occurrence of incomplete nest building and misplaced eggs in nests of other bird species. The thiamine deficiency may be induced either by a causative agent(s) acting directly on the affected individual, by reduced uptake of thiamine, and/or by insufficient transfer of thiamine between the trophic levels in the food web. Further studies will focus on thiamine levels in the food for these birds, as well as factors involved in the high mortality of juvenile eider ducklings.

Nutrient deficit among Swedish wildlife

Balk, L.; Hägerroth, P.-Å.; Tjärnlund, U.; Åkerman, G.; Gustavsson, H.; Ström, K.; Ström, M.; Ruiz, Y.; Mörner, T.; Sigg, L.; Hansson, T.
2013 | Swedish University of Agricultural Sciences (SLU) (9-9)

Moose Health: Management challenges with growing ungulate populations | October 24, 2013 | Uppsala, Sweden

Thiamine (vitamin B1) is a water-soluble vitamin essential for all living cells. In the cell, thiamine is phosphorylated to thiamine diphosphate, which functions as a cofactor for at least five life sustaining enzymes in the cellular metabolism. Previous studies have shown that sub-lethal thiamine deficiency in vertebrates gives rise to a large number of health effects, such as reduced feeding, memory and learning disturbances, immune suppression, and damage to the blood-brain barrier, as well as altered carbohydrate, protein, and lipid metabolism.

During the last decades, thiamine deficiency has been observed in various animal classes such as fish, birds, and reptiles. Methods to discover and characterize thiamine deficiency among wildlife include analysis of thiamine concentrations and thiamine ratios between various tissues, measurement of thiamine dependent enzyme activities and percentage of apoenzyme, as well as thiamine treatment of thiamine deficient animals (i.e. response to treatment).

Hanöbukten, a bay in southern Sweden, where thiamine (vitamin B1) deficiency cannot be excluded as the primary cause of the ecosystem disturbance

Balk, L.; Hägerroth, P.-Å.; Sigg, L.; Karlsson, S.; Tjärnlund, U.; Åkerman, G.; Gustavsson, H.; Ström, K.; Ruiz, Y.; Ström, M.; Mörner, T.; Hansson, T.
2013 | Ålakademin (35-35)

VATTEN13 : Vad har hänt med vattnet i Hanöbukten? | November 21, 2013 | Åhus, Sweden

Hanöbukten is a large bay at the east coast of the County of Skåne in southern Sweden. It faces the Baltic Sea just south of the waters and archipelago of the County of Blekinge.

During a period of approximately 6–10 years, residents fishing in Hanöbukten have observed an alarming decline in the fish abundance. In fact, the decline is so severe that many local fishermen have given up their profession and sold their boats and equipment, even in cases where their families have been fishing in Hanöbukten for many generations.

These observations have resulted in a public enquiry about the situation in Hanöbukten (Anonymous 2013), executed by the staff at the Swedish Agency for Marine and Water Management (HaV) as a commission from the Swedish government.

The public enquiry of Hanöbukten (Anonymous 2013) indicates that the problems have appeared in recent years, and according to local fishermen, the problems occur in episodes. Hence, it is very interesting that the thiamine deficiency, documented in fish and birds close to Hanöbukten, also occur in episodes and is the only known disorder today with dire consequences for individual specimens as well as entire populations.

The thiamine deficiency may be caused by one, today unknown, substance by a certain biochemical mechanism. Thiamine has a central role in the cellular metabolism of e.g. sugar, lipids, and protein, and thiamine deficiency may compromise several physiological functions, such as the immune defence, vision and hearing, long and short time memory functions, the blood brain barrier, reproduction, temperature regulation, nerve function, reproduction, and survival. Our knowledge so far makes thiamine deficiency a plausible cause for the ongoing disturbance of the ecosystem in Hanöbukten.

On this foundation, we suggest an investigation of thiamine status in some well-characterised vertebrate model-species to elucidate whether biota in Hanöbukten suffer from thiamine deficiency or not.

Reference: Anonymous (2013) Hanöbukten. Regeringsuppdrag. Havs- och vattenmyndighetens rapport 2013-10-31. Havs- och vattenmyndigheten, Göteborg, Sweden, 107 pp.

Lethal thiamine deficiency in several bird species in the Baltic Sea

Balk, L.; Hägerroth, P.-Å.; Hansson, T.; Tjärnlund, U.; Gustavsson, H.; Mörner, T.; Åkerman, G.
2012 | Clin. Chem. Lab. Med. | 50 (A64-A65) | ISBN: ISSN: 1434-6621

Advances and Controversies in B-Vitamins and Choline | September 19, 2019 | Leipzig, Germany

Thiamine deficiency has recently been demonstrated in several species of wild birds, both adults and newly hatched young, in connection with extensive mortality in a paralytic disease in the Baltic Sea. This thiamine deficiency may be the dominating cause of the observed population declines in many bird species during the last three decades. Accordingly, the need for an understanding of this problem is urgent.

Our research team has found reduced thiamine concentrations in the egg-yolk, liver, and brain, as well as reduced activities of the thiamine-dependent enzymes transketolase and alpha-ketoglutarate dehydrogenase in the liver and brain. In these organs, there were also very high proportions of apoenzyme of these enzymes. The thiamine status of females in the field was critical for the degree of breeding failure. The many observations of advanced thiamine deficiency in adult birds strongly suggest that also varying degree of moderate thiamine deficiency occurs among the affected species.

One effect of moderate thiamine deficiency is altered behaviour. We have made plenty of observations of reduced aggressiveness and low noise level in bird colonies, as well as incomplete nest building and egg laying in nests of other species. The observed degree of thiamine deficiency suggests that the birds also suffer from weakening of the blood-brain barrier and immune suppression. This is not only an obvious threat to ecosystem sustainability. For example, infectious diseases may be more easily spread to humans by immunosuppressed birds. The thiamine deficiency may be induced either by a causative agent(s) acting directly on the affected individual, and/or by insufficient transfer of thiamine between the trophic levels in the food web.

Is this normal?

Mörner, T.; Carlsson, L.; Hägerroth, P.-Å.; Balk, L.
2012 | Wildlife Disease Association (WDA) (399-399)

Joint 61st WDA / 10th Biennial EWDA Conference: Convergence in Wildlife Health | July 24, 2012 | Lyon, France

It is a well known fact that female birds can lay their eggs in nests of other birds. This behavior can be observed in birds within the same species and is then called intraspecific nest-parasitism. This is observed in ducks such as common goldeneye (Bucephala clangula) and ruddy duck (Oxyura jamaicensis). Interspecific nestparasitism is when birds place their eggs in nests of other species, like the cuckoo (Cuculus canorus) . Nest-parasitism is by many ecologists regarded as a normal behavior and explained in different ways. However, we have during studies of thiamine (vitamin B1) deficiency since 2005 at several localities in the Baltic sea, in gulls (Laridae sp.) and common eider ducks (Somateria mollissima) among other sea birds, observed an increasing number of eggs from one species placed in nests of another species. During this study, on one affected island in Blekinge archipelago (southern Sweden) there were eggs from other species observed in nests of common eider, barnacle goose (Branta leucopsis), herring gull (Larus argentatus), mallard (Anas platyrhynchos), Canada goose (B. canadensis) and mute swan (Cygnus olor) in a percentage between 2 and 15 per cent of the nests. This high misplacing percentage of eggs among these species has not been observed back in time at localities along the Swedish coastline in the Baltic Sea. We have also observed foreign items such as stones and bits of plastic waste in nests of gulls, geese, swans and ducks, that the birds apparently have collected to include into the clutch. Although some ecologists may regard this behavior as normal, we consider the observed placing of eggs in nests of other species in this seabird colony as unnatural, since the offspring most certainly will die from starvation and/or other erroneous attendance of the adult parent(s). Thiamine deficiency is well-known to cause damaged brain functions, including altered behavior. Since we have found severe thiamine deficiency in both adult birds and chicks of ducks, geese and gulls from islands where this behavior is observed, our main working hypothesis is that this egg-laying disorder may have its origin in the deficiency of thiamine. The relationship between misplacing of eggs and thiamine deficiency will be further studied.

Effects of thiamine deficiency on eiders

2011 | Gotland University

International workshop on sea ducks and their food | September 19, 2019 | Visby, Gotland, Sweden

Vilken roll spelar sjukdomen fågeldöden?

2011 | Stiftelsen Sveriges Vildnad

Vad har hänt med våra skärgårdsfåglar? Vart tar ejdern vägen? | May 18, 2011 | Stockholm, Sweden

Thiamine deficiency in the ecosystem

Balk, L.; Hägerroth, P.-Å.; Hansson, T.; Tjärnlund, U.; Gustavsson, H.; Mörner, T.; Åkerman, G.
2011 | Swedish University of Agricultural Sciences (SLU) (43-43) | ISBN: 978-91-576-9057-9 | Report No: CRU Report 26

Reproductive Disorders in Baltic Vertebrate Wildlife (BALTREP 2011) | September 19, 2019 | Uppsala, Sweden

Thiamine, vitamin B1, is a water-soluble vitamin that is essential for vertebrates. Inside the cell, thiamine is phosphorylated to thiamine diphosphate, which functions as a cofactor for at least 5 life sustaining enzymes in the cellular metabolism. Previous studies have shown that sub-lethal thiamine deficiency in vertebrates may give rise to a large number of health effects, such as reduced feeding, memory and learning disturbances, immune suppression, and damage to the blood-brain barrier. Relationships have also been demonstrated between thiamine deficiency and altered lipid metabolism and neurodegenerative diseases.

Thiamine deficiency was recently demonstrated in several species of wild birds that are dying in large numbers from a paralytic disease in the Baltic Sea area. The egg, liver, and brain had reduced thiamine concentrations, and the liver and brain had reduced activities of the thiamine-dependent enzymes. In the liver and brain, there were also elevated proportions of apoenzyme, i.e. enzyme without the thiamine diphosphate cofactor. Moreover, paralyzed individuals were successfully remedied by thiamine treatment. Excess mortality and breeding failure were linked to a thiamine deficiency syndrome, which most probably has contributed significantly to declines in many bird populations during the last decades. Both adults and juveniles are subject to excess mortality, and breeding failure is caused by several factors, such as reduced number of eggs, reduced chick survival, and altered behavior, including rudimentary nest building, reduced aggression rates (attack diving), and low noise level in the colonies.

The thiamine deficiency may be induced either by a causative agent(s) acting directly on the affected individual, and/or by insufficient transfer of thiamine between the trophic levels in the food web. Classical persistent organic pollutants are not primarily suspected, since the affected species occupy a wide range of ecological niches and positions in the food web. The authors stress that they are open to the possibility that other wildlife, beside fish and birds, may suffer from thiamine deficiency as well.

Reply to Rocke and Barker: The question is not whether birds are affected by thiamine deficiency or botulism, it is about the order of events

Balk, L.; Hägerroth, P.-Å.; Åkerman, G.; Hanson, M.; Tjärnlund, U.; Hansson, T.; Hallgrimsson, G.T.; Zebühr, Y.; Broman, D.; Mörner, T.; Sundberg, H.
2010 | Proc. Natl. Acad. Sci. U.S.A. | 107 (11) (E37-E37)

Overview of the paper “Wild birds of declining European species are dying from a thiamine deficiency syndrome”

Balk, L.; Hägerroth, P.-Å.; Åkerman, G.; Hanson, M.; Tjärnlund, U.; Hansson, T.; Hallgrimsson, G.T.; Zebühr, Y.; Broman, D.; Mörner, T.; Sundberg, H.
2010 | Maj and Tor Nessling Foundation (15-15)

The global environmental change - Messages from birds - Sixth environment symposium of the Maj and Tor Nessling Foundation in cooperation with BirdLife Finland | September 19, 2019 | Hanasaari, Espoo, Finland

Wild birds of several species are dying in large numbers from a paralytic disease with hitherto unknown cause in the Baltic Sea area. A research team at Stockholm University, Sweden, has demonstrated strong relalionships between this disease, breeding failure, and advanced thiamine (vitamin B1) deficiency in eggs, young, and adults. The results are presented in the article "Wild birds of declining European species are dying from a thiamine deficiency syndrome", published in the Proc Natl Acad Sci USA, 2009, 106, 12001-12006.

Thiamine is an essential nutrient for birds and other vertebrates. In the living cell, its phosphorylated form acts as a cofactor for several life sustaining enzymes, which are non-functional if the cofactor is missing. Thiamine is also necessary for the proper functioning of the nerves. Thiamine deficiency was demonstrated in the egg, liver, and brain as reduced thiamine concentrations, and in the liver and brain as reduced activities of the thiamine-dependent enzymes. In the liver and brain, there were also elevated proportions of these enzymes without the thiamine cofactor. Moreover, paralysed individuals were successfully remedied by thiamine treatment. The excess mortality and breeding failure are part of a thiamine deficiency syndrome, which most probably has contributed significantly to declines in many bird populations during the last decades.

The authors stress the urgent need of further investigations focusing on causation. The thiamine deficiency may be induced either by a causative agent(s) acting directly on the affected individual, and/or by insufficient transfer of thiamine between the trophic levels in the food web. Classical persistent organic pollutants are not primarily suspected, since the affected species occupy a wide range of ecological niches and positions in the food web. Last but not least, the authors stress that they are open to the possibility that other wildlife may suffer from thiamine deficiency as well.

Overview of the paper “Wild birds of declining European species are dying from a thiamine deficiency syndrome”

Balk, L.; Hägerroth, P.-Å.; Åkerman, G.; Hanson, M.; Tjärnlund, U.; Hansson, T.; Hallgrimsson, G.T.; Zebühr, Y.; Broman, D.; Mörner, T.; Sundberg, H.; Tillitt, D.
2010 | Great Lakes Fisheries Commission (GLFC)

Thiamine Deficiency Workshop, Great Lakes Fisheries Commission | September 19, 2019 | Ann Arbor, MI, USA

Wild birds of several species are dying in large numbers from a paralytic disease with hitherto unknown cause in the Baltic Sea area. A research team at Stockholm University, Sweden, led by Associate Professor Lennart Balk, has demonstrated strong relationships between this disease, breeding failure, and advanced thiamine (vitamin B1) deficiency in eggs, young, and adults. The results are presented in the article “Wild birds of declining European species are dying from a thiamine deficiency syndrome”, published in the Proc Natl Acad Sci USA, 2009, 106, 12001-12006.

Thiamine is an essential nutrient for birds and other vertebrates. In the living cell, its phosphorylated form acts as a cofactor for several life sustaining enzymes, which are non-functional if the cofactor is missing. Thiamine is also necessary for the proper functioning of the nerves. Thiamine deficiency was demonstrated in the egg, liver, and brain as reduced thiamine concentrations, and in the liver and brain as reduced activities of the thiamine-dependent enzymes. In the liver and brain, there were also elevated proportions of these enzymes without the thiamine cofactor. Moreover, paralysed individuals were successfully remedied by thiamine treatment. The excess mortality and breeding failure are part of a thiamine deficiency syndrome, which most probably has contributed significantly to declines in many bird populations during the last decades.

The authors’ primary aim has been to demonstrate the relationship between the paralytic disease and thiamine deficiency. Also important has been to form an idea about the geographical distribution of the thiamine deficiency syndrome and its distribution among species. Advanced thiamine deficiency was demonstrated in the Baltic Sea area, but incipient thiamine deficiency was found also in Iceland.

The paralytic disease was observed in 78% of the investigated bird species (28 of 36). In some species, such as the herring gull, thiamine deficiency results in a reduction of the number of eggs, whereas in other species, such as the common eider, the females seem to be capable of producing eggs essentially devoid of thiamine. As a result, many herring gulls in the Baltic Sea area do not produce any eggs at all, and the excess mortality among common eider young is immense.

The many observations of advanced thiamine deficiency strongly suggest that also varying degree of moderate thiamine deficiency occurs among the affected species. One effect of moderate thiamine deficiency is altered behaviour. The authors report plenty of observations of reduced aggressiveness and low noise level in herring gull colonies, as well as incomplete nest building in several species. Another effect of moderate thiamine deficiency is immune suppression. The avian influenza is just one example of a disease that may spread more easily among thiamine-deficient birds. Moreover, thiamine deficiency may weaken the blood-brain barrier, which normally protects the brain from many toxic substances.

The occurrence of paralysis among birds has received some attention previously, but has usually been attributed to botulinum poisoning, which is caused by a bacterium. The authors demonstrate that thiamine deficiency is the actual cause. The problem of excess mortality and breeding failure among birds has also received some attention previously, and has routinely been attributed to lack of food, even when reliable information concerning the food supply has been limited. The authors show that thiamine deficiency causes starvation as a consequence of loss of appetite, whereas starvation itself does not result in thiamine deficiency.

The authors stress the urgent need of further investigations focusing on causation. The thiamine deficiency may be induced either by a causative agent(s) acting directly on the affected individual, and/or by insufficient transfer of thiamine between the trophic levels in the food web. Classical persistent organic pollutants are not primarily suspected, since the affected species occupy a wide range of ecological niches and positions in the food web. Last but not least, the authors stress that they are open to the possibility that other wildlife may suffer from thiamine deficiency as well.

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